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Title (Primary) Algal remodeling in a ubiquitous planktonic photosymbiosis
Author Decelle, J.; Stryhanyuk, H.; Gallet, B.; Veronesi, G.; Schmidt, M.; Balzano, S.; Marro, S.; Uwizeye, C.; Jouneau, P.-H.; Lupette, J.; Jouhet, J.; Maillot-Maréchal, E.; Schwab, Y.; Schieber, N.L.; Tucoulou, R.; Richnow, H.; Finazzi, G.; Musat, N.;
Journal Current Biology
Year 2019
Department ISOBIO;
Volume 29
Issue 6
Language englisch;
POF III (all) T41;
Keywords symbiosis; plankton; microalga; single-cell imaging; photosynthesis; mass spectrometry imaging; 3D electron microscopy; eukaryotes; plastid; Phaeocystis
Abstract Photosymbiosis between single-celled hosts and microalgae is common in oceanic plankton, especially in oligotrophic surface waters. However, the functioning of this ecologically important cell-cell interaction and the subcellular mechanisms allowing the host to accommodate and benefit from its microalgae remain enigmatic. Here, using a combination of quantitative single-cell structural and chemical imaging techniques (FIB-SEM, nanoSIMS, Synchrotron X-ray fluorescence), we show that the structural organization, physiology, and trophic status of the algal symbionts (the haptophyte Phaeocystis) significantly change within their acantharian hosts compared to their free-living phase in culture. In symbiosis, algal cell division is blocked, photosynthesis is enhanced, and cell volume is increased by up to 10-fold with a higher number of plastids (from 2 to up to 30) and thylakoid membranes. The multiplication of plastids can lead to a 38-fold increase of the total plastid volume in a cell. Subcellular mapping of nutrients (nitrogen and phosphorous) and their stoichiometric ratios shows that symbiotic algae are impoverished in phosphorous and suggests a higher investment in energy-acquisition machinery rather than in growth. Nanoscale imaging also showed that the host supplies a substantial amount of trace metals (e.g., iron and cobalt), which are stored in algal vacuoles at high concentrations (up to 660 ppm). Sulfur mapping reveals a high concentration in algal vacuoles that may be a source of antioxidant molecules. Overall, this study unveils an unprecedented morphological and metabolic transformation of microalgae following their integration into a host, and it suggests that this widespread symbiosis is a farming strategy wherein the host engulfs and exploits microalgae.
ID 21716
Persistent UFZ Identifier https://www.ufz.de/index.php?en=20939&ufzPublicationIdentifier=21716
Decelle, J., Stryhanyuk, H., Gallet, B., Veronesi, G., Schmidt, M., Balzano, S., Marro, S., Uwizeye, C., Jouneau, P.-H., Lupette, J., Jouhet, J., Maillot-Maréchal, E., Schwab, Y., Schieber, N.L., Tucoulou, R., Richnow, H., Finazzi, G., Musat, N. (2019):
Algal remodeling in a ubiquitous planktonic photosymbiosis
Curr. Biol. 29 (6), 968 - 978.e4